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Ubiquitination of stalled ribosome triggers ribosome-associated quality control

Author

Listed:
  • Yoshitaka Matsuo

    (Tohoku University)

  • Ken Ikeuchi

    (Tohoku University)

  • Yasushi Saeki

    (Tokyo Metropolitan Institute of Medical Science)

  • Shintaro Iwasaki

    (University of California
    RIKEN)

  • Christian Schmidt

    (University of Munich)

  • Tsuyoshi Udagawa

    (Tohoku University)

  • Fumiya Sato

    (Tohoku University)

  • Hikaru Tsuchiya

    (Tokyo Metropolitan Institute of Medical Science)

  • Thomas Becker

    (University of Munich)

  • Keiji Tanaka

    (Tokyo Metropolitan Institute of Medical Science)

  • Nicholas T. Ingolia

    (University of California)

  • Roland Beckmann

    (University of Munich)

  • Toshifumi Inada

    (Tohoku University)

Abstract

Translation arrest by polybasic sequences induces ribosome stalling, and the arrest product is degraded by the ribosome-mediated quality control (RQC) system. Here we report that ubiquitination of the 40S ribosomal protein uS10 by the E3 ubiquitin ligase Hel2 (or RQT1) is required for RQC. We identify a RQC-trigger (RQT) subcomplex composed of the RNA helicase-family protein Slh1/Rqt2, the ubiquitin-binding protein Cue3/Rqt3, and yKR023W/Rqt4 that is required for RQC. The defects in RQC of the RQT mutants correlate with sensitivity to anisomycin, which stalls ribosome at the rotated form. Cryo-electron microscopy analysis reveals that Hel2-bound ribosome are dominantly the rotated form with hybrid tRNAs. Ribosome profiling reveals that ribosomes stalled at the rotated state with specific pairs of codons at P-A sites serve as RQC substrates. Rqt1 specifically ubiquitinates these arrested ribosomes to target them to the RQT complex, allowing subsequent RQC reactions including dissociation of the stalled ribosome into subunits.

Suggested Citation

  • Yoshitaka Matsuo & Ken Ikeuchi & Yasushi Saeki & Shintaro Iwasaki & Christian Schmidt & Tsuyoshi Udagawa & Fumiya Sato & Hikaru Tsuchiya & Thomas Becker & Keiji Tanaka & Nicholas T. Ingolia & Roland B, 2017. "Ubiquitination of stalled ribosome triggers ribosome-associated quality control," Nature Communications, Nature, vol. 8(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:8:y:2017:i:1:d:10.1038_s41467-017-00188-1
    DOI: 10.1038/s41467-017-00188-1
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    Cited by:

    1. Momoko Narita & Timo Denk & Yoshitaka Matsuo & Takato Sugiyama & Chisato Kikuguchi & Sota Ito & Nichika Sato & Toru Suzuki & Satoshi Hashimoto & Iva Machová & Petr Tesina & Roland Beckmann & Toshifumi, 2022. "A distinct mammalian disome collision interface harbors K63-linked polyubiquitination of uS10 to trigger hRQT-mediated subunit dissociation," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    2. Ken Ikeuchi & Nives Ivic & Robert Buschauer & Jingdong Cheng & Thomas Fröhlich & Yoshitaka Matsuo & Otto Berninghausen & Toshifumi Inada & Thomas Becker & Roland Beckmann, 2023. "Molecular basis for recognition and deubiquitination of 40S ribosomes by Otu2," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Junqiao Jia & Tarek Hilal & Katherine E. Bohnsack & Aleksandar Chernev & Ning Tsao & Juliane Bethmann & Aruna Arumugam & Lane Parmely & Nicole Holton & Bernhard Loll & Nima Mosammaparast & Markus T. B, 2023. "Extended DNA threading through a dual-engine motor module of the activating signal co-integrator 1 complex," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Malgorzata J. Latallo & Shaopeng Wang & Daoyuan Dong & Blake Nelson & Nathan M. Livingston & Rong Wu & Ning Zhao & Timothy J. Stasevich & Michael C. Bassik & Shuying Sun & Bin Wu, 2023. "Single-molecule imaging reveals distinct elongation and frameshifting dynamics between frames of expanded RNA repeats in C9ORF72-ALS/FTD," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    5. Yoshitaka Matsuo & Takayuki Uchihashi & Toshifumi Inada, 2023. "Decoding of the ubiquitin code for clearance of colliding ribosomes by the RQT complex," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    6. Ji Geng & Shuangxi Li & Yu Li & Zhihao Wu & Sunil Bhurtel & Suman Rimal & Danish Khan & Rani Ohja & Onn Brandman & Bingwei Lu, 2024. "Stalled translation by mitochondrial stress upregulates a CNOT4-ZNF598 ribosomal quality control pathway important for tissue homeostasis," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    7. Yosuke Ito & Yuhei Chadani & Tatsuya Niwa & Ayako Yamakawa & Kodai Machida & Hiroaki Imataka & Hideki Taguchi, 2022. "Nascent peptide-induced translation discontinuation in eukaryotes impacts biased amino acid usage in proteomes," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    8. Katharina Best & Ken Ikeuchi & Lukas Kater & Daniel Best & Joanna Musial & Yoshitaka Matsuo & Otto Berninghausen & Thomas Becker & Toshifumi Inada & Roland Beckmann, 2023. "Structural basis for clearing of ribosome collisions by the RQT complex," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    9. Jiangnan Liu & Noemi Nagy & Carlos Ayala-Torres & Francisco Aguilar-Alonso & Francisco Morais-Esteves & Shanshan Xu & Maria G. Masucci, 2023. "Remodeling of the ribosomal quality control and integrated stress response by viral ubiquitin deconjugases," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    10. Xiaolu Wang & Yao Li & Xiaojie Yan & Qing Yang & Bing Zhang & Ying Zhang & Xinxin Yuan & Chenhao Jiang & Dongxing Chen & Quanyan Liu & Tong Liu & Wenyi Mi & Ying Yu & Cheng Dong, 2023. "Recognition of an Ala-rich C-degron by the E3 ligase Pirh2," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

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